In: Marshes
Editors: D. C. Abreu et al.
ISBN 978-1-61942-715-0
© 2012 Nova Science Publishers, Inc.
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Chapter 1
RECONSIDERING CLIMATIC ROLES
OF MARSHES: ARE THEY SINKS OR
SOURCES OF GREENHOUSE GASES?
Serena Moseman-Valtierra
University of Rhode Island, Department of Biological Sciences,
Kingston, RI, US
ABSTRACT
Marshes are exceptionally productive ecosystems that constitute
significant global carbon sinks. Particularly along coasts, marshes are
prime targets for efforts that aim to enhance biological carbon
sequestration. However, the net climatic impact of ecosystems depends
not only on carbon sinks but also on sources of carbon and nitrogen to the
atmosphere. Carbon dioxide (CO2), methane (CH4), and nitrous oxide
(N2O) strongly influence climate together; CH4 and N2O wield 25 and
298 times the global warming potential per molecule as CO2,
respectively, over 100 year time periods. Yet, the magnitude of all three
greenhouse gases has rarely been measured simultaneously in marshes,
and controls on these fluxes are not well understood. Anthropogenic
impacts such as nutrient loading and other changes in environmental
conditions may substantially alter the greenhouse gas emissions from
marsh ecosystems. Recent manipulative experiments show that short-term
nitrate loading (at concentrations found in anthropogenically enriched
groundwater) can significantly enhance emissions of N2O from salt marsh
sediments. These fluxes are substantial enough in terms of global
2
Serena Moseman-Valtierra
warming potential to offset as much as half of the daily C sequestration
rates in coastal marshes. This is in striking contrast to negative fluxes
(sinks) of N2O that are consistently observed in the absence of nitrate
(Moseman-Valtierra et al. 2011). In general, studies so far suggest that
the highest N2O fluxes are found in marshes experiencing significant
anthropogenic nutrient loading. Since nitrate loading affects many
riparian and coastal marshes worldwide, the net global warming potential
of marshes may be substantially altered on local scales, with potential
consequences for global climate. However, in several marshes N 2O and
CH4 fluxes show high spatial heterogeneity that suggests complex
controlling factors. Current research is reviewed herein to identify
known environmental controls of N2O and CH4 production, consumption,
and emission from fresh and coastal marshes. This information is used to
develop hypotheses regarding potential shifts in greenhouse gas sinks and
sources in response to rising sea levels, increasing temperatures, and
biological invasions. Information regarding anthropogenic and
environmental factors that affect greenhouse gas emissions in marsh
ecosystems is essential in order to prioritize areas for conservation and to
guide restoration activities across dynamic fresh-marine transition zones
and shifting biomes. As restoration activites proceed, the ability of marsh
ecosystems to not just passively respond to global climate change but also
to actively influence climate through carbon sequestration and
greenhouse gas emissions, needs to be recognized, especially as these
abilities may be significantly altered by human activities.
INTRODUCTION
In wetlands spanning a range of ecosystems and latitudes, from the fringes
of boreal lakes and rivers to temperate coastal salt marshes, vascular plants
dominate and define marsh landscapes. Marsh grasses and sedges display
impressive productivity given the relatively stressful wetland environment that
results from regular inundation of soils (Mitsch and Gosselink 2001). Salt
marshes, in particular, rank among the world‟s most productive ecosystems
(Mitsch and Gosselink 2001). This remarkable productivity is supported, in
part, by regular tidal flushing that reduces the accumulation of reduced toxins
in salt marsh soils while also delivering limiting nutrients from coastal waters.
The significance of coastal wetland productivity to surrounding
ecosystems was historically described in Odum‟s classic hypothesis that these
ecosystems produce an excess of organic matter which is exported to the sea,
where it supports coastal fisheries (Odum 1980). For decades since,
researchers tested this hypothesis by evaluating the C budgets of marsh
Reconsidering Climatic Roles of Marshes
3
ecosystems and the relationship between marsh primary production and
coastal fisheries (i.e. Morris and Whiting 1986, Dela Cruz 1973, Teal 1962).
However, evidence was not conclusive that all coastal wetlands represent
significant sources of carbon to the adjacent ocean. Rather, C exports from
coastal marshes seemed to be contingent upon factors such as tidal amplitude
and hydrology, and the hypothesis continues to be evaluated, particularly, in
the context of wetland subsidence and hypoxia (Das et al. 2011). In contrast to
the relative emphasis on evaluating marshes as potential sources of carbon to
adjacent waters via lateral fluxes (outwelling), the role of marshes in vertical
(soil-atmosphere) biogeochemical fluxes has been relatively ignored- until
now.
Growing concern over anthropogenic impacts on global climate, via
emissions of greenhouse gases, has led to efforts to identify potential sites for
biological C sequestration, and attention is increasingly turning to coastal
marshes. Wetlands store at least 44.6 Tg C y-1 globally (Chmura et al. 2003),
representing the largest terrestrial biological carbon pool. Initial attention was
directed to freshwater wetlands as carbon sinks, particularly northern
peatlands, however salt marshes (and mangroves) have been found to store
carbon more rapidly per unit area (Chmura et al. 2003). The estimated average
rate of carbon sequestration in salt marshes and mangrove swamps (which did
not significantly differ from each other) is 201 g CO2 m-2 y-1, which is an order
or magnitude higher than C sequestration in peatlands (20-30 g CO2 m-2 y-1)
(Chmura et al.2003, Roulet 2000).
An additional attraction of coastal marshes as potential sites of biological
sequestration is that they have been considered to produce insignificant
emissions of the potent greenhouse gases, methane and nitrous oxide. Like
CO2, methane and nitrous oxide have increased significantly above preindustrial levels, rising by 48% and 18%, respectively. In contrast, however,
they wield 25 and 298 times the global warming potential per molecule as CO2
over a 100 year period (Forster et al. 2007), which raises concerns about
anthropogenic and natural sources of these gases. Salt marshes are thought to
constitute small sources of methane because methanogens cannot compete
with sulfate-reducing bacteria that thrive in coastal marsh soils (Fenchel and
Blackburn 1979, Morris and Whiting 1986). They have also not been
considered major sources of N2O, at least in part because this is a minor
product of denitrification (Seitzinger 1988, Kaplan et al. 1979). However,
measurements of N2O and CH4 in European coastal waters have frequently
revealed that estuaries, which include marshes, are a net source of N2O to the
atmosphere, contributing up to 26% of global oceanic N2O emissions, and a
4
Serena Moseman-Valtierra
significant source of CH4 as well (Bange 2006). Specific measurements in
coastal marshes within such estuaries have rarely been made and thus their
contributions to estuarine greenhouse gas emissions remain largely unknown.
Thus, the assumption that coastal marshes do not constitute major sources of
greenhouse gases has persisted despite relatively few in situ measurements.
Given that biological C sequestration in coastal marshes could be
substantially offset by such greenhouse gas emissions from these ecosystems,
the relative significance of these processes needs to be quantified and
understood. As management decisions regarding wetland restorations are
made, cost-benefit analyses will need to consider the potential for
enhancement of greenhouse gas emissions in estuaries where wetland area is
expanded (Andrews et al. 2006), and the environmental factors that would
maximize or minimize those emissions need to be better understood (Huang
and Pant 2009, Andrews et al. 2006).
The purpose of this review is to summarize what is known about the
magnitude and controls of greenhouse gas emissions from marshes. As few
measurements have been made in coastal salt marshes, I compare greenhouse
gas emissions from a range of fresh and marine marshes to those of other
ecosystems in which significant fluxes have been reported. At least one recent
review has focused on greenhouse gas emissions from relatively pristine
coastal ecosystems (Dalal and Allen 2009), so this review intentionally
includes greenhouse gas fluxes from anthropogenically-impacted marshes
which may substantially differ from undisturbed marshes. Given growing
human populations and their indelible roles in many ecosystems, estimates of
greenhouse gas emissions and our understanding of their controls will need to
be based on studies that incorporate human impacts.
MICROBIAL SOURCES OF GREENHOUSE GASES
IN MARSH SOILS
Marsh soils provide a heterogeneous environment with combinations of
aerobic and anaerobic niches in which microbial respiration proceeds (Sutton
Grier et al. 2011). While CO2 is produced from most respiratory processes (by
microbes, plants and animals), N2O and CH4 are produced by more specific
microbial guilds. The net product of production and consumption of these
gases, by both aerobic and anaerobic processes, is their emission from marsh
soils to the atmosphere.
Reconsidering Climatic Roles of Marshes
5
N2O: Nitrous oxide is a byproduct of very diverse nitrogen transformations,
although the two main sources in coastal marshes are thought to be
nitrification and denitrification. Nitrification is generally an aerobic pathway
by which NH4+ is oxidized in two steps, first to NO2-, and then to NO3-. Both
bacteria and archaea perform the first step of nitrification (oxidation of
ammonium), which is the rate limiting step of the process due to close
coupling of nitrite-oxidizing bacteria with the ammonia oxidizers (Ward 2005,
Ward et al 2007, Konneke et al. 2005). The pathways of N2O production by
nitrifiers are not well understood. One is nitrifier denitrification in which
nitrite is reduced to nitric oxide (NO) and N2O under microaerobic conditions
(Wrage et al. 2001, Arp and Stein 2003). While nitrification by autotrophs is
an aerobic process, the process of nitrifier denitrification (also by autotrophs)
seems to be enhanced as O2 levels decrease, perhaps because it is a mechanism
for acquiring energy under O2- limited conditions (Arp and Stein 2003, Wrage
et al. 2001). Ammonium provides the electron source for nitrifier
denitrification (Kool et al. 2011, Ritchie and Nicholas 1972; Bock et al.,
1995). Polypeptides capable of catalyzing the reduction of nitrite in nitrifier
denitrification include the blue copper cytochrome c oxidase (Miller and
Nicholas 1985) and an unidentified copper-containing enzyme (Arp and Stein
2003, Ritchie and Nicholas 1974). Potential controls on nitrifier-denitrification
have been reviewed elsewhere (Wrage et al. 2001) and are thought to include
high N content of soils or sediments, low organic C content, and possibly low
pH, based on thermodynamic considerations (Wrage et al. 2001). Depending
upon availability of various electron acceptors, denitrification can be a major
respiratory pathway by which anaerobic heterotrophs respire organic carbon
after oxygen has been exhausted as a terminal electron acceptor. N2O is an
intermediate prior to the last step in denitrification, with the complete process
proceeding as follows: NO3 NO2-  NO  N2O  N2 (Hochstein and
Tomlinson 1988, Wrage et al. 2001). Typically N2 is the dominant product of
denitrification, with N2O:N2 ratios being less than 0.5% in estuarine sediments
(Seitzinger and Kroeze 1998), but this varies with environmental conditions
(discussed further below). Denitrification can be performed by diverse
microbes including archaea and eukarya (Zumft 1997), although most studies
of the microbial communities in marsh soils have focused on patterns of
functional bacterial genes involved in denitrification (Bowen et al. 2011, Cao
et al. 2008, Dandie et al. 2011) which have been found to be similar among
bacteria and archaea (Cabello et al. 2004).
6
Serena Moseman-Valtierra
N2
CO2
N2O
CH4
O2
CH4
N2O
CO2
N2O
Gut
microflora
NH3 or NH4+
Methanogenesis
O2
NH4+
NO2NO3-
Methanogenesis
NO2O2
O2
O2
NO3-
N2O
CH3COOH
N2O
O2
O2
Denitrification
O2
Organic C
Denitrification
Belowground
Figure 1. Diagram of major processes producing greenhouse gases in marsh soils,
including plant-mediated transport of gases to the atmosphere and faunal production of
greenhouse gases. Red text (and boxes) indicate anaerobic processes. Blue text (and
boxes) indicate anaerobic processes.
In coastal ecosystems, nitrification and denitrification are frequently
coupled, with nitrifiers providing the NO3- that denitrifiers reduce to N2O and
then N2 (Hamersley and Howes 2005, Jenkins and Kemp 1984). Important
sites where this coupling occurs include rhizospheres (roots and immediately
surrounding soils), where sufficient oxygen is introduced to sediments by plant
photosynthesis to enable nitrification to occur (Lovell 2005), and in
microniches such as animal burrows and tubes (Kristensen and Kostka 2005)
(Figure 1). Due to the coupling of nitrification and denitrification, the relative
importance of each as sources of the greenhouse gas N2O can be tricky to
determine. Further, the significance of each process is likely to vary in
response to shifts in environmental conditions. For example, in laboratory
manipulations of inundation regimes with intertidal sediment cores,
nitrification was found to be the dominant source of N2O during relatively
dessicated conditions, while denitrification was the major source under
waterlogged or reflooded conditions, and highest N2O concentrations were
observed in the sediments under the latter conditions (Hou et al. 2007). In
Reconsidering Climatic Roles of Marshes
7
addition to variation with water levels, rates of nitrification can show
seasonality that is distinct from denitrification, as observed in a freshwater
marsh where the former was maximal in May while the latter reached highest
rates in September (Gribsholt et al. 2006). Other processes that can produce
nitrous oxide include dissimilatory reduction to ammonium (DNRA) (Smith
and Zimmerman 1981) and assimilatory nitrate reduction although the relative
significance of these sources, and nitrifier denitrification (Wrage et al. 2001),
has not been well quantified compared to nitrification and denitrification in
marshes. In soils, assimilatory nitrate reduction is less than 6% of total nitrate
reduction, indicating that it may also be an insignificant source of N2O
(Venterea and Rolston 2000, Dalal and Allen 2009).
CH4: Methanogenesis constitutes the last terminal respiratory pathway by
which organic matter is degraded, because it yields less energy than alternative
pathways. Methanogens include a diverse range of bacteria and archaea that
use a wide array of various carbon sources and range in habitats from soils to
microbial mats and animal guts. The carbon substrates that methanogens
convert into methane have been determined predominantly via cultures and
can be classified into 3 groups: CO2-type substrates, methyl substrates, and
acetotrophic substrates (Madigan and Martinko 2006). These substrates are
made available by fermentative bacteria that degrade polymeric material into
labile forms. The predominant substrate supporting methanogenesis in marsh
soils can vary with temperature (Wagner and Pfeiffer 1997). Much of the
methane in saline marshes is thought to be derived from methyl compounds,
such as trimethylamine and dimethylsulfide, although H2 is an important
substrate in surfaces of microbial mats in a salt marsh (Buckley et al. 2008). In
salt marshes, groups of methanogenic bacteria have been found to vary in their
use of different substrates, with some using trimethylamine but not H2 or
acetate, others using H2 but not trimethylamine or acetate, and some that could
use isopropanol, H2, and formate (Franklin et al. 1988), which suggests that
niche partitioning may occur among them. In freshwater sediments,
methanethiol, dimethyl sulfide, and methanol are known to be degraded by
methanogens (Lomans et al. 2001). There is evidence that groups of
methanogens using different substrates may compete with each other, which
includes the finding that addition of acetates to peatland soils inhibited
hydrogenotrophic methanogenesis (Brauer et al. 2004, Liu et al. 2011).
Although methanogenesis is an anaerobic process, methanogens have
been found in oxic marsh soil layers (Wagner and Pfeiffer 1997), and they
likely interact with aerobic and anaerobic methanotrophs. Methanogenic
archaea have been found to be most abundant in surface soils of multiple
8
Serena Moseman-Valtierra
freshwater marshes (Liu et al. 2011). Abundance estimates of methanogens in
the latter study were based on real-time PCR analyses of DNA and thus may
reflect dead or inactive archea (Liu et al. 2011), so further studies are needed
to determine whether methanogens can be active in what seem to be aerobic
sediments (possibly by residing in anaerobic microniches). The overall flux of
methane from marsh soils will represent the interaction of methanogens with
methanotrophic bacteria that oxidize methane, in aerobic microhabitats such as
rhizospheres, as well as in anoxic environments where sulfate reduction can be
coupled to methane oxidation (Conrad 1996). Anaerobic methane oxidation
has also relatively recently been found to occur via consortia that couple the
process to denitrification (Dalal and Allen 2009, Raghoebarsing et al. 2006,
Islas-Lima 2004) as well as to iron reduction (Sivan et al. 2011).
Current knowledge regarding environmental controls on nitrous oxide
production and consumption as well as methanogenesis and methane oxidation
are discussed further in the following sections.
OVERVIEW OF THE MAGNITUDE
OF GREENHOUSE GASES IN MARSHES
A summary of N2O fluxes reported from a range of northern hemisphere
freshwater marshes are provided in Table 1, and studies which measured N2O
fluxes (along with CO2 and CH4) in coastal marshes are found in Table 2. The
studies summarized in these tables are not exhaustive of all published
literature addressing greenhouse gas production, but they do represent the
geographical range of marshes in which in situ fluxes are mostly being
measured. All of the studies that are summarized in Tables 1-3 were conducted
via in situ closed chamber techniques, and units have been converted to enable
comparison of the greenhouse gas fluxes. One exception is Roobroeck et al.
2010 (which used core-based incubations of marsh soils) which is included
because no comparable in situ studies of fens with N enrichment are known.
CO2 fluxes are included where they were reported, although controls on CO2
are not the focus of this review because they have been relatively well
characterized (Wigand et al. 2009, Rocha and Goulden 2008, Drake et al.
1996, Morris and Whiting 1986, Morris and Whiting 1985).
Table 1. N2O fluxes (g N2O m-2 h-1) from freshwater marshes (standard errors in parentheses)
Source
dominant plant(s)
Wetland description
Location
Jordan et al. 2007
n/a
Weller et al. 1994
Yu et al. 2007
Deyeuxia angustifolia
FW, FT, NT; spring
FW, FT, NT; summer
FW, FT, NT; fall
FW, RV, NT; spring
FW, R, NT; summer
FW, R, NT; fall
FW, RP, FST
FW
FW
FW, F
USA Chesapeake Bay
USA Chesapeake Bay
USA Chesapeake Bay
USA Chesapeake Bay
USA Chesapeake Bay
USA Chesapeake Bay
USA Maryland
NE China
NE China
Biebrza, Poland
FW, F
FW, F
FW, FST, +N
Biebrza, Poland
Biebrza, Poland
Netherlands
FW, G, +N
B,C
Netherlands
Baltic Sea
Roobroek et al. 2010
Hefting et al. 2003
Carex appoprinquata,
Peucedanum palustre
Alnus glutinosa
Glyceria maxima
Liikanen et al. 2009
average N2O
flux
0.2 (0.3)
0.7(0.4)
1.2 (0.8)
4.2(3.1)
1.6 (1.2)
5.4 (2.8)
4.4
4.45 to 6.85
-1.00 to -0.76
2.1 (0.3)
-3.0 (0.1)
2.7 (0.4)
358
maximum:
4167
36 to 72
-5.5
Minimum and maximum values are included where they have been provided by the sources. The key to the wetland
descriptions, which are based on the respective authors’ evaluations of their field sites, is as follows: FW=Freshwater, C=
Coastal, SM= salt marsh, BRK= Brackish marsh, CRK= Tidal creek, F=fen, FST= Forested, RV=Riverine, RP= Riparian,
G=grassland, FT= Flat, B=Boreal, +N= Fertilized with nitrogen, SAND= sandy intertidal.
Table 2. Average fluxes of greenhouse gases from coastal and freshwater marshes and wetlands
(with standard errors in parentheses)
Roobroek et
al. 2010
Carex appoprinquata
Notes
CO2 max
CO2min
(mg CO2 m-2 h-1)
average CO2 flux
max. CH4
min. CH4
(mg CH4 m-2 h-1)
average CH4 flux
max. N2O
min. N2O
(gN2O m-2 h-1)
Biebrza,
Poland
2.1 (0.3)
35(3)
Tussock
FW, F
Biebrza,
Poland
Biebrza,
Poland
Biebrza,
Poland
USA New
York
-3.0 (0.1)
21(9)
Hollows
2.7 (0.4)
36(9)
16 (2.9)
20(8)
Tussock
+1N nitrate
Hollows +
0.1N nitrate
FW, F
FW, F
MosemanSpartina patens
Valtierra et al.
2011
average N2O flux
FW, F
Peucedanum palustre
Hopfensperger
et al. 2009
Location
Wetland
description
dominant plant(s)
Source
FW,
RP,
FST
C, SM,
+N
C, SM
5.4 (2.8)
10
-0.06
0.15
USA( MA) 71 (24)
0
224
0.14
(0.1)
0
0.56
USA(MA)
-94
56
0.05
(0.05)
-0.24
0.32
-6 (8)
37
380
(47)
367
Transparent
chambers +
300 M
nitrate
Controls,
dark and
transparent
chambers
MosemanValtierra et al
in prep.
Hirota et al.
2007
Ferron et al.
2007
Magenheimer
et al. 1996
DeLaune et al.
1983
Kristensen et
al. 2008
Morris and
Whiting 1985
Spartina patens
Carex rugulosa, Phragmites
australis
C, SM,
+N
USA(MA)
191 (74)
C, SM
USA(MA)
C, SM
0.3(0.1)
0
0.64
380
(158)
1.81(12.1) -18.3 94
0.01
(0.004)
-0.04
0.1
294
(117)
USA(MA)
2.37(2.4)
0.0
9
0.01
(0.007)
0
0.03
163
(127)
C, SM
Japan
20
-10
60
91
245
C, SM
Japan
-10
-30
1
SAND
Japan
30
20
50
0.01
0.34
14
44
114
0.02
0.1
134 325
0.01
0.5
C, CRK Spain
C, SM
USA east
coast
C, BRK USA east
coast
MNG, Tanzania
FST
MNG, Tanzania
CRK
MNG, Tanzania
CRK
C, SM USA east
coast(North
Inlet, SC)
4
410
Dark
chambers +
300 M
nitrate
100 425 fertilized
marsh
37
320
35
0.1
314 reference
marsh, see
Deegan et
al. 2007
-23
725
104
75
13
154
11.1
0.4
0.00
0.06
51
211
0.01
0.1
2
11
0.07
0.2
55
147 low tide
high tide
226
(46)
Minimum and maximum values are included if provided by the sources. The key to the wetland descriptions, which are based on respective authors‟ evaluations of their field
sites, is as follows: FW=Freshwater, C= Coastal, SM= salt marsh, BRK= Brackish marsh, CRK= Tidal creek, F=fen, FST= Forested, RV=Riverine, RP= Riparian,
G=grassland, FT= Flat, B=Boreal, +N= Fertilized with nitrogen, SAND= sandy.
Table 3. Average methane fluxes in marshes (with standard errors in parentheses)
Source
Dominant plant(s)
Wetland
description
Location
Average CH4 flux
(mg CH4 m-2 h-1)
min.
CH4
Bartlett et al.
1987
S.alterniflora
C, SM
2.1 (0.66)
1.9
S. alterniflora and S.
cynosuroides
C, BRK
S. cynosuroides
C, BRK
FW
USA
Chesapeake
Bay
USA
Chesapeake
Bay
USA
Chesapeake
Bay
USA
(Louisiana)
USA
(Louisiana)
USA
(Louisiana)
China
3.0
0.16
10
FW
FW
China
Switzerland
19.6
1.18
0.1
55
20
DeLaune et al.
1983
C, BRK
C, BRK
C, BRK
Ding et al.
2005
Flury et al.
2010
Carex muliensis,
Carex meyeriana
Carex spp.
Phragmites australis
max. CH4
Notes
2.6 (0.39)
0.6 (0.08)
11
0.7
salinity 18
11.1
salinity 1.4
24.3
salinity 0.4
Sha et al. 2011
Kankaala et al.
2004
VanDerNat
and
Middleberg
2000
Mitsch et al.
2010
Not reported but see
Altor and Mitsch
2006)
FW, RV
Switzerland
0.3
86
FW, CRT
FW, OX
Switzerland
Switzerland
20
0.1
Phragmites australis
B, LK
Finland
0.02
0.04
0.5
Typha latifolia and
Phragmites australis
B, LK
Finland
1.3
47
Typha latifolia and
Phragmites australis
B,LK
Finland
1.4
19
Scirpus lacustris
BRK
Belgium
0.5
Phragmites australis
BRK
Belgium
9
Not reported
TROP
Costa Rica
60
Raphia taedigera
TROP
Costa Rica
7 to 15
49
Seasonally
flooded
tropical site
Humid
tropical site
Minimum and maximum values are included where they have been provided by the sources. The key to the wetland descriptions, which
are based on authors‟ evaluations of their field sites, is as follows: FW=Freshwater, C= Coastal, SM= salt marsh, BRK= Brackish
marsh, CRK= Tidal creek, F=fen, FST= Forested, RV=Riverine, RP= Riparian, G=grassland, FT= Flat, B=Boreal, +N= Fertilized
with nitrogen, SAN D= sandy intertidal.
Table 4. Conceptual summary of impacts of several environmental factors on N2O production
(via aerobic and anaerobic processes), N2O consumption, and CH4 production and consumption in marsh soils
Environmental
factor
Aerobic N2O
production
(nitrification)
Anaerobic N2O
production
(incomplete
Denitrification)
+
-/+
-/+
N2O
consumption
(complete
denitrification)
+/0
+
Methane
production
Methane
consumption
Reactive N
+
+/0
oxygen
+
+
Water level
+
(inundation)
Salinity
-?
-?
-/+??
?
Sulfate/Sulfide
?
+
-?
-/+?
+?
Temperature
+
+
+?
+
+?
“+” indicates a positive relationship, “-“ denotes a negative relationship. “?” indicates cases where relationships are unclear due to lack
of investigation or contradictory results thus far.
Reconsidering Climatic Roles of Marshes
15
Among the papers reviewed, the largest N2O fluxes have been found in
systems in which anthropogenic N loading is occurring (Hefting et al. 2003,
Table 1; Moseman-Valtierra et al. 2011 and Ferron et al 2007 in Table 2). In
un-enriched fresh and coastal marshes, N2O emissions are generally low, and
even negative, while significant positive N2O fluxes are found in N enriched
marshes (discussed further below). Although marshes are replaced by
mangroves at lower latitudes, and mangroves are not included in this review,
there is generally a lack of measurements of greenhouse gas emissions in
tropical coastal ecosystems, as discussed elsewhere (Dalal and Allen 2009).
Most studies have not yet been able to attribute the N2O fluxes to specific
microbial sources, although the importance of various N transformation is
known to vary with water content of the soils (Hou et al. 2011, Dalal and
Allen 2009), as described further below.
CH4 emissions from marshes (in Tables 2 and 3) show a considerable
range in magnitudes both across and within marshes. The prevalent notion that
salt marshes constitute small sources of methane relative to their freshwater
counterparts is not always consistently supported. Within an estuarine system,
CH4 fluxes from marshes do show inverse relationships with salinity (Bartlett
et al. 1987, DeLaune et al. 1983, Table 3) but across marshes, several
freshwater systems show small methane emissions (Sha et al. 2011,
Hopfensperger et al. 2009) including tropical mangroves (Kristensen et al.
2008, Table 2), while some notably high CH4 fluxes have been measured in
coastal salt marshes (Hirota et al. 2007, DeLaune et al. 1983).
Many environmental factors co-vary in space and time in dynamic marsh
environments. The following section will address some of the key factors that
affect greenhouse gas emissions from marshes, with the understanding that
isolating the influence of a single variable is challenging, and that many
factors interactively influence the biogeochemistry and ecology of marshes. A
summary of the general relationships between the discussed environmental
factors and production or consumption of N2O and CH4 is provided in Table 4.
ROLES OF ANTHROPOGENIC N LOADING
ON GHGS IN MARSHES
A recent review of greenhouse gas (GHG) emissions from more than 100
studies in terrestrial ecosystems revealed that although anthropogenic N
enrichment increases the terrestrial C sink, it stimulates CH4 and N2O
16
Serena Moseman-Valtierra
emissions to an extent that can largely offset that effect in multiple ecosystems
(Liu and Greaver 2009). Global N2O emissions from aquatic ecosystems were
estimated to be 1.9 Tg N yr-1, using nitrification and denitrification rates from
rivers, estuaries, and continental shelves along with models of N loading from
177 watersheds (Seitzinger and Kroeze 1998). These estimates were based on
measurements of N2O:N2 ratios produced by denitrification in mesocosms
with estuarine sediments exposed to different N loading rates (Seitzinger and
Nixon 1985). In that estuarine study, N2O:N2 ratios were found to increase
linearly with N loading over a range of 100 mol N m-2 h-1 to 3645 mol N
m-2 h-1 (Seitzinger and Nixon 1985). In many estuarine sediments, N2O:N2
ratios are generally within 0.1-0.5%, with highest ratios (about 6%) observed
in heavily polluted sediments (Seitzinger and Kroeze 1998). This ratio is
significant because it indicates the extent to which denitrification is completed,
and if there are large increases in the production of the greenhouse gas N2O
relative to the unreactive gas N2 in ecosystems with high rates of
denitrification, then they may have significant feedbacks on climate.
Notably, no specific estimates of marsh contribution to global N2O
emissions have been made. Relatively few studies have actually measured
impacts of anthropogenic N loading on GHG fluxes or N2O:N2 ratios of gases
emitted from marshes, despite their key roles in water purification as they
intercept nutrient loads in rivers, run-off, groundwater, and atmospheric
deposition. In salt marsh sediments, the ratio of N2O:N2 produced by
denitrification has been observed to vary greatly, between 5% and 50%, (Lee
et al. 1997). The lowest ratio (<5%) was observed in sediments collected from
a salt marsh experiencing the highest inputs of 624 kg N ha-1 yr-1 (Lee et al.
1997). This pattern of decreasing N2O:N2 ratios in marshes with increasing N
loads, suggests that although N2O production increases with NO3- loading, the
release of N2O relative to N2 may decrease. N loads in this study varied by an
order of magnitude (with maximal rates in Childs River, MA) and lowest at
Sage Lot Pond, Waquoit Bay (MA) where N loads were estimated to be only
64 kg N ha-1 y-1(Lee et al. 1997). More research is needed to understand what
controls the tremendous variability in N2O yields in coastal ecosystems and to
ascertain what factors besides N may make the N2O:N2 ratio vary greatly in
marshes in particular.
Methane emissions show less of a clear response to nitrogen inputs. In an
experimental nitrate enrichment experiment within a freshwater marsh, no
change in methane emissions was observed, although high variability in
diffusive and ebullitive fluxes was noted (Flury et al. 2010). However,
ammonium is known to be able to inhibit methane oxidation in soils and
Reconsidering Climatic Roles of Marshes
17
cultures (Conrad 1996, Steudler et al. 1989). The mechanism for this inhibition
involves similarities of the enzyme that catalyzes methane oxidation (methane
monooxygenase) with ammonium monooxygenase (used by nitrifying
bacteria). Ammonium can be oxidized via the methane monooxygenase
enzyme, and if it does so, then it decreases enzymes available for methane
oxidation (Bodelier and Laanbroek 2004). Nitrifying bacteria are known to be
able to oxidize methane at atmospheric concentrations, and that activity
declines at ammonium concentrations equivalent to or higher than those
present in temperate forest soils (Steudler et al. 1989). Additional studies are
needed to determine conditions under which such an inhibition of methane
oxidation may exist in marshes, but it is important for understanding what
controls the size of methane sinks (and therefore the magnitude of methane
sources) of these ecosystems. Possibly, ammonium inhibition of methane
oxidation is restricted to marshes created for wastewater treatment and
microniches in which ammonium concentrations are quite high (Laanbroek
2010).
Principal factors influencing the extent to which N2O and other
greenhouse gas emissions vary in response to N loading include the magnitude
and duration of the N inputs to marsh ecosystems. Experimental nitrate pulses
(single additions equivalent to 1.4 g N m-2) added to Spartina patens marsh
plots were found to significantly increase N2O fluxes over 3 dates (MosemanValtierra et al 2011, Table 2). As control (unfertilized plots) and background
N2O fluxes were consistently low or negative, the addition of nitrate (at levels
comparable to highly enriched groundwater that is found in anthropogenicallyimpacted estuaries in region) constituted a shift of the wetland sediments from
sinks of N2O to sources of N2O in response to this short-term fertilization. In
sediment cores collected from hollows of a Carex appoprinquata-dominated
fen, single nitrate amendments (at levels near daily atmospheric nitrate
deposition) changed hollows from sinks to sources of N2O as well. Responses
to nitrate additions produced only a minor increase in N2O in cores collected
from tussocks of the same site, which was thought to be due to the influence of
plant roots in competing more strongly for mineral N in those sediments than
in those collected from relatively bare hollows (Roobroeck et al. 2010).
Responses of sediments to pulsed nutrients may differ substantially from
those to chronic N inputs for several reasons. Microbial responses to pulse
nutrients may reflect changes in enzymatic activities, while population sizes
and possibly community composition may shift over time periods involved in
chronic N loading or other long term changes such as land use regimes (Ma et
al. 2008). Further, plant competition may limit microbial responses to nutrient
18
Serena Moseman-Valtierra
inputs over short terms, but over longer periods of time, chronic N loads can
cause shifts in plant community composition, or diminish plant biomass
allocation belowground (Langley et al. 2009), which could reduce the extent
of interaction or competition between microbes and plants. Chronic nutrient
loading may also lead to shifts in many environmental properties that
indirectly influence microbial responses to nitrogen inputs, such as oxygen
levels, oxidation-reduction potential of soils, and marsh elevation or
inundation levels if chronic nutrient loading contributes to marsh subsidence.
Chronic nitrogen loading currently affects many ecosystems, and thus its
impact on marsh biogeochemistry and greenhouse gas emissions needs to be
better understood. Exceptionally high N2O fluxes were observed in chronically
nitrate-loaded riparian buffer zones, where nitrous oxide fluxes in forested
zones (dominated by Alnus glutinosa ) with higher nitrate concentrations (2330 mg N L-1) in groundwater exceeded those in grassland buffer zones (with
Glyceria maxima) with lower nitrate concentrations (4-9 mg N L-1) (Hefting et
al. 2003, Table 1). Similarly, in Narragansett Bay, RI, soil respiration rates
were found to significantly increase across salt marshes experiencing a
gradient of watershed nitrogen loads (from 10 kg N ha-1 y-1 to 6727 kg N ha-1
y-1) (Wigand et al. 2009). In Spartina alterniflora zones of these marshes,
surface soils declined in %C and %N content as respiration rates increased,
suggesting that some of the labile organic matter in these soils was being
turned over by microbial activities (Wigand et al. 2009). However, in contrast
to studies of pulsed nutrient inputs, nitrous oxide fluxes in a chronically
fertilized S. patens marsh with more than 7 years of experimental fertilization
via enrichment of tidal creek waters (Deegan et al. 2007) did not significantly
differ from an adjacent reference (unfertilized) marsh (Moseman-Valtierra et
al. in prep., Table 2).
Physical factors of the environment may constrain impacts of chronic
nutrient loading on marshes. The heavily nutrient-loaded Child‟s River in
Cape Cod, MA, which is enriched by septic tank effluent, was found to be
supersaturated with N2O in surface waters, but due to stratification of the
water, benthic sediments displayed consumption of N2O in most flux
measurements and were thought to have only limited exposure to nitrate-rich
surface waters (LaMontagne et al. 2003). Likewise, if hydrological and
physical characteristics of rivers or estuaries constrain the extent of interaction
between nutrient-rich water and marsh soils, then emissions of N2O may not
be significantly enhanced (Groffman et al. 1998).
Recognizing the extent of anthropogenic alteration of greenhouse gas
fluxes will be important in marshes that have high nutrient loads. Significant
Reconsidering Climatic Roles of Marshes
19
N2O fluxes were estimated from a salt marsh in Spain, in which fish farm
effluent was draining into the tidal creek (Ferron et al. 2007). Groundwater in
coastal and riparian marshes is frequently found to have high concentrations of
N2O and CH4 (Kroeger et al. in prep., Groffman et al. 1998), as well as high
levels of anthropogenic N (Kroeger et al. 2006, Kroeger et al. 2007), and when
it intercepts marshes, it can be difficult to determine whether the gases were
produced in marsh sediments or subterranean groundwater (Groffman et al.
1998). Recognizing the site of production would be a key first step in
mitigating the emissions. Tropical coastal margins, where marshes may be
largely replaced by mangrove forests, may face particularly high levels of N
loading due to rapid urban growth and large human populations. In the Adyar
River in SE India, organic rich and ammonium-enriched regions were found to
have high methane and nitrous oxide fluxes, with annual estimates being
equivalent in global warming potential to one month of CO2 emissions from
motor vehicles in the region (Rajkumar et al. 2008).
Summary
Some of the highest N2O fluxes have been observed in marsh ecosystems
with significant N loading, and they are sufficient to substantially offset C
sinks (as observed in several other ecosystems) (Liu and Greaver 2009).
Marshes show much wider ranges in N2O:N2 ratios produced by denitrification
compared to other ecosystems, and impacts of N loading and other
environmental factors on this ratio need to be better understood. Methane
emissions in theory could be enhanced by higher ammonium levels, due to
inhibition of methane oxidation, but field studies have not yet demonstrated
this relationship. The magnitude and duration of anthropogenic N inputs exerts
a considerable influence on net N2O, CO2, and CH4 emissions, and the
fundamental influence of human impacts on release of these greenhouse gases
from marsh ecosystems should be recognized. In particular, shifts in GHG
fluxes need to be compared to changes in net C sequestration (that may also
vary in response to anthropogenic N loading), in order to estimate potential net
feedbacks of marshes on global climate change.
20
Serena Moseman-Valtierra
OXYGEN AND WATER INUNDATION
Tidal inundation influences the extent and depth to which oxygen
penetrates marsh soils. Nutrient enrichment of tidal or groundwater inputs
(discussed above) can result in hypoxic or anoxic conditions via
eutrophication, and nutrient loading may possibly exacerbate physical
limitations (such as tidal inundation) on oxygen availability in marshes.
Photosynthetic activities of plants and other primary producers (micro- and
macroalgae, cyanobacteria) introduce oxygen to marsh soils (in mats on the
sediment surface or deeper in plant rhizospheres, see “Plant Influences”).
These photosynthetic activities respond to changes in light levels on diel and
seasonal time scales. Animal burrows and tubes and biogenic irrigation
activities (associated with feeding) can also increase the depth to which
oxygen penetrates marsh soils as well as increase the area of oxic-anoxic
boundaries across which nutrients and other solutes are exchanged (Kristensen
and Kostka 2005, Figure 1). These are the microenvironments in which
microbial respiration, potentially yielding or consuming greenhouse gases,
takes place.
Oxygen is commonly manipulated in laboratory experiments to test its
influence on N2O emissions. For example, the oxygen content of purging gas
used in experiments with fen soil cores was found to significantly affect N2O
emissions (Roobroeck et al. 2010). Among soils purged with no O2, 1%, or 5%
O2, N2O production was greatest in soils with the highest amount of oxygen,
regardless of soil type (Roobroeck et al. 2010), and this was attributed to the
inhibition of nitrous oxide reductase by oxygen (McKenney et al. 1994).
In the field, several studies have supported relationships between oxygen
availability and nitrous oxide emissions, due to the influence of oxygen on
nitrification and/or denitrification rates. Oxygen is known to be a proximal
controller of denitrification, although direct measurements of oxygen in the
environment have been limited (Burgin et al. 2010). Differences in oxygen
availability were used to explain higher N2O emissions found at night than
during the day in estuarine sediments using closed chamber techniques (Jensen
et al. 1984). Parallel studies had shown maximal denitrification rates in these
sediments at night when oxygen-generating photosynthetic activities ceased
(Andersen et al. 1984, Jensen et al. 1984). Thus denitrification was thought to
be the major source of N2O emissions from these sediments (Jensen et al.
1984). The aerobic process of nitrification, on the other hand, has been thought
to only be possible in soils with oxidation-reduction potentials above 200 mV
(Wanderborght and Billen 1975), which has been used to explain the limited
Reconsidering Climatic Roles of Marshes
21
vertical distribution of nitrification to the top cm of intertidal sediment cores
(Hou et al. 2007), although marsh sediments in situ will have more complexity
due to the influence of plants and animals. Positive relationships between
nitrous oxide consumption in coastal sediments and oxygen uptake (measured
in terms of flux rates, La Montagne et al. 2002) were observed and attributed
to use of N2O as an electron acceptor during hypoxic conditions (LaMontagne
et al. 2003). Thus fully anaerobic conditions seemed to favor the most
complete denitrification of nitrate to N2. Likewise, in a freshwater wetland,
N2O fluxes were higher in Deyeuxia marsh plots with no water logging than in
seasonally waterlogged plots (Yu et al. 2007). Although neither were major
sources of N2O, the seasonally waterlogged marsh plots acted as sinks of N2O,
in contrast to the plots that were not water logged (which were always net
sources of N2O). Several studies have suggested that because wetland soils are
less dry (and less oxic) than other aerated soils, N2O fluxes may be smaller
because denitrification proceeds more completely with a larger percent of N2O
going to N2 (Yu et al. 2010, Lindau et al. 1991, Samuelsson 1985, Schiller and
Hastie 1994, Smith et al. 1983).
Oxygen is also strongly related to methane production and emissions in
marshes, given that methanogenesis is an anaerobic process. When oxygen is
introduced to marsh sediments by plant roots or animal burrows and tubes, it
sustains alternative electron acceptors in the sediment that can be used in
mineralization and thereby represses methanogenesis (reviewed in Laanbroek
2010). Methane emissions have shown diel variation (Kaki et al. 2001). Also,
methane fluxes have been found to be higher in continuously inundated zones
of a created freshwater marsh than zones with pulsed flooding (Altor and
Mitsch 2008). In field measurements, dissolved methane concentrations in
marsh water and ebullition of methane from the sediment of a Phragmites
australis freshwater marsh were both negatively related to water column
dissolved oxygen (Flury et al. 2010). Further, methane release from these
marsh sediments was suggested to form a positive feedback in which dissolved
oxygen was reduced in the water column above the marsh, thereby reducing
oxygen fluxes into the sediment where methane was formed, which could
positively influence methane production (Flury et al. 2010).
Manipulations of soil inundation regimes offer indirect tests of the effects
of oxygen on CH4 and N2O production. Mesocosms with S. alterniflora plants
in salt marsh sediments that were permanently inundated produced higher CH4
fluxes than others which were only intermittently inundated (Ding et al. 2010).
In this experiment, inundation was sustained for one growing season and did
not significantly affect plant biomass or stem density, but it did significantly
22
Serena Moseman-Valtierra
reduce sediment redox potential (Ding et al. 2010). Therefore, the increase in
CH4 fluxes from inundated sediments was attributed to a favorable (reduced)
environment for methanogenesis. In contrast, at least one study found that
periodically inundated S. alterniflora mesocosms released more CH4 (7-86%
more) than permanently inundated mesocosms (Cheng et al. 2007). However,
the standing water in mesocosms of that study was 10 cm, in contrast to the 5
cm depth maintained by Ding et al. (2010), and the difference in results may
have been in part due to the role of water in acting as a barrier of gases,
slowing their diffusion to the atmosphere (Cheng et al. 2007), rather than a
fundamental difference in response to oxygen availability. In a core-based test
of the impact of inundation on N2O in intertidal sediments, highest N2O
concentrations were observed in reflooded sediments following a 10day period
of emersion (under a ventilating fan) rather than in those with long term (5
day) immersion or emersion (10 days) alone. These time periods reflected
average periods of immersion during spring tides in high intertidal flats.
Measurements of nitrification and denitrification rates in these cores revealed
that during emersion, most N2O was produced by the former, while during
immersion the latter process dominates (Hou et al. 2007), which is consistent
with the control of oxygen availability on both processes. Nitrate
concentrations were also highest in the reflooded sediments than in other
treatments. As in intertidal sediments, moisture levels strongly mediate the
sources of observed N2O fluxes from soils, with N2O coming predominantly
from nitrification up to a threshold of about 65% water-filled pore space in
soils (Dalal and Allen 2009, Dalal et al. 2003.). Combinations of isotopic
enrichments and inhibition techniques have been applied successfully in silt
loam soils, showing that denitrification can account for all of N2O with 70%
water filled pore spaces, but that nitrification can account for up to 81% of all
N2O emitted from soils with only 60% water filled pore spaces (Bateman and
Baggs 2005). Such techniques seem to remain to be applied in marsh
sediments.
Effects of oxygen on greenhouse gas emissions have also been inferred
from manipulations of light levels. In contrasts of transparent (light) and
opaque (dark) chambers, N2O consumption (via denitrification) was
significantly less in transparent (light) chambers placed over unvegetated
coastal sediments than in opaque (dark) chambers (LaMontagne et al. 2003).
This is in contrast however to observations of higher N2O fluxes (and thus less
consumption) in opaque rather than transparent chambers within a S. patens
marsh during a short-term nitrate enrichment experiment (Moseman-Valtierra
et al. 2011). Possibly the presence of plants in the latter study, which would
Reconsidering Climatic Roles of Marshes
23
compete more strongly with microbes for nitrogen in the presence of light,
explains why N2O fluxes were lower than they were in opaque chambers. In
the case where plants are absent and thus microbes may have less competition
for nutrients, oxygen may exert a stronger influence on N2O fluxes than
nitrogen availability.
Summary
Oxygen may stimulate N2O production from aerobic processes
(nitrification), which due to coupling with denitrification in many coastal
marshes, may indirectly favor anaerobic N2O production as well (Table 4).
However, as oxygen levels increase, overall rates of denitrification (an
anaerobic process) decline. Under completely anoxic conditions,
denitrification tends to proceed completely to N2 rather than N2O (Table 4).
Therefore, intermediate levels of oxygen likely result in highest N2O fluxes.
The relationship of methane to oxygen is simpler, as oxygen inhibits
methanogenesis but promotes methane oxidation (Table 4).
PH
The pH level of marsh soils can be a function of oxygenation and
inundation, with pH decreasing as oxygen levels decline and sulfide
compounds accumulate, and pH is known to strongly influence greenhouse gas
emissions from soils. Historical legacies of nutrient enrichment or acidification
from atmospheric inputs to aquatic ecosystems can also influence pH levels in
riparian and coastal marshes (Monteith et al., 2007, Fenner et al. 2011).
Due to the influence of pH on microbial nitrogen transformations, it may
alter N2O emissions. In soils, pH is known to affect overall rates of
denitrification as well as the ratio of N2O:N2 produced by denitrification
(Cuhel and Simek 2011, Simek and Cooper 2002). Based on studies of
cultures of denitrifiers, optimal denitrification rates have been found near
neutral pH (Van Den Heuvel 2011, Tomsen et al. 1994) while the portion of
N2O produced by denitrification has been seen to increase as pH declines (Van
den Heugel et al. 2010, Thomsen et al. 1994). Likewise, in soils, higher
denitrification rates have been found in alkaline soils than in acidic ones, while
the fraction of gaseous product represented by N2O (relative to N2O + N2) was
highest in acidic soils (Cuhel and Simek 2011). The increase in proportion of
24
Serena Moseman-Valtierra
N2O produced in denitrification has been attributed to negative effects of low
pH (at values of pH=5) on genes for nitrite reductase (nirS) and nitric oxide
reductase (cnorB) Saleh-Lakha et al. 2009) and is thought to involve a posttranscriptional mechanism (Liu et al. 2010). In organic-rich and nitrateamended riparian soils, a longer period of N2O production was observed in
slurries with pH values adjusted to 4 rather than slurries with pH values of 7
(Van den Heuvel 2011). These results were supported by field studies in the
riparian site, where N2O emissions were highest (comprising 77% of all N2O
emissions) in spots with pH ranging from 4-5 (with an overall site pH ranging
from 3.9 to 6.6). However, not all field studies have shown the same
relationships to pH (Cuhel et al. 2010, Bandibas et al. 1994), likely because
multiple factors influence whether N2O production translates into N2O
emissions, including changes in N2O reduction and physical barriers of gas
transport to the atmosphere (Van den Heuvel 2011). Interestingly,
manipulations of pH in slurries of pasture soils revealed that current pH levels
of soils affected ratios of N2O: (N2O+N2) more strongly than historical pH
conditions (which reflected different soil management regimes), although the
latter showed significant relationships to potential denitrification (DEA) rates
(Cuhel and Simek 2011). Further studies are needed to discern how pH
changes differentially affect other nitrogen transformations and the source of
N2O emissions from marshes. Mechanistic understanding may necessitate
characterization of the major microbial communities, as the diverse microbes
involved in processes such as nitrification may show different responses to pH
(i.e. Cao et al. 2011).
Methane emissions from marshes also show some relationships with pH.
In contrast to N2O, lower methane emissions have been found in northern
acidic (pH<5.5) tundra ecosystems of Alaska than in relatively neutral
(pH>6.5) southern ecosystems. As with N2O, however, the importance of pH
has not yet been isolated from other co-varying factors in these ecosystems. In
particular, the northern tundra ecosystems also have less heat flux, shallower
thaw depths, and smaller C sinks (Zona et al. 2011) than their southern
counterparts. Nonetheless, within a recently re-flooded Sphagnum and Juncus
wetland, methane and dissolved organic C “hotspots” were observed in sites
with high pH values (pH 5.1 to 5.3) relative to other sites (pH 4.8 to 4.9)
(Fenner et al. 2011). Also, on a smaller scale, pH was found to be higher in
low centers of “polygons” in the Arctic tundra soils, and that corresponded to
higher dissolved CO2 levels in the wet surface soils. This counter-intutive
pattern was possibly caused by trapping of CO2 by the water (which acted as a
diffusion barrier) or by accumulation of vascular plant material in the center of
Reconsidering Climatic Roles of Marshes
25
the microtopographic structure which reduced redox (Zona et al. 2011).
Negative relationships are known to exist between oxidation of soils and pH
(Reddy and DeLaune 2008). Methane emissions were not measured in that
particular study (Zona et al. 2011). Finally, the relationship between methane
emissions and pH are known to vary between temperate and tropical wetlands
(Inubushi et al. 2005). In a temperate wetland in Japan, where pH values
ranged between 5 and 7, methane emissions were positively related to pH, but
that was not the case in a tropical forested wetland in Indonesia where soils
had been drained and the pH was less than 5 (Inubushi et al. 2005). Positive
relationships between pH and methane emissions have been described also in
Canadian wetlands (Valentine et al. 1994). In general, however, studies are
needed to characterize the response of all major greenhouse gases to changes
in pH, and manipulative approaches may be essential for understanding
mechanism by which pH mediates greenhouse gas emissions.
Summary
The effect of pH varies for N2O and CH4 emissions in marshes.
Denitrification, a major source of N2O emissions from marsh soils, is highest
at neutral pH, however the N2O yield of denitrification (relative to N2)
increases in acidic pH conditions. Further studies need to determine how pH
changes affect the variety of other nitrogen transformations that can produce
N2O emissions in marshes. For methane, in contrast, higher emissions have
been observed in marshes (tundra) when pH is closer to neutral than in acidic
soils. However, the positive relationship between pH and methane emissions is
not observed in tropical wetlands where pH values were below 5. The lack of
consistent relationships between pH and greenhouse gas emissions may thus
involve differences in the ranges of pH between sites (and latitudes) and well
as the influence of numerous co-varying factors (moisture, oxidation reduction
potential) that also modify greenhouse gas emissions in situ.
SALINITY
Methane fluxes display strong inverse relationships with salinity in the
porewater of marsh soils (Magenheimer et al. 1996) due to the dominance of
sulfate-reducing bacteria over methanogens in saline waters. For this reason,
methane fluxes from salt marshes have predominantly been considered to be
26
Serena Moseman-Valtierra
negligible, based on relatively few in situ measurements (i.e. Ding et al 2004,
Magenheimer et al. 1996). Nonetheless, methane fluxes from marshes have
been found to be highly variable, often for reasons that are not well understood
(Table 3). For example, in a salt marsh in the Bay of Fundy, the combination
of salinity and water table position could only explain 29% of the variance in
CH4 emissions (in contrast to CO2 emissions for which 63% of variance could
be correlated with aboveground plant biomass and water table position)
(Magenheimer et al. 1996). Further, somet measurements of methane fluxes in
salt marshes are not insignificant (Hirota et al. 2007, Table 2), and recent
experiments suggest that responses of methane to salt water intrusion may be
complex (Weston et al. 2011).
Salinity has a less direct effect on nitrous oxide fluxes. Concentrations of
dissolved greenhouse gases in the tidal creek of a salt marsh receiving effluent
from a fish farm were always highest during low tides (Ferron et al. 2007),
which is when salinity levels tend to be lowest. However, that low salinity
(reflecting freshwater input from the fish farm effluent) also coincides with
higher nitrogen inputs to the marsh (Ferron et al. 2007), and thus the effect of
salinity cannot be determined in isolation. Similar correlations of N2O with
low salinity and high nitrate concentrations have been described in numerous
estuaries (Wang et al. 2009, LaMontagne et al. 2003, Barnes and Owens
1998). In laboratory studies with oligohaline estuarine sediment, cores
incubated with higher salinity water were found to have higher ammonium
fluxes than those with about 8-9 psu lower salinity levels (with overall salinity
ranges between 0 and 19 psu), although N2O fluxes were not measured. These
differences were sustained for 6 days despite no overall difference in
respiration rates between the salinity treatments (Giblin et al. 2010).
Relationships between salinity and denitrification rates were observed on
seasonal scales, with higher denitrification rates generally being found in
spring than summer (Giblin et al. 2010). The opposite pattern was observed for
dissimilatory nitrate reduction to ammonium, which was very low in the spring
but higher in the summer, following patterns of salinity in the estuary (Giblin
et al. 2010). Given the significant changes in estuarine nitrogen
transformations in response to salinity shifts, further research ought to address
the relative significance of DNRA, denitrification, and other nitrogen
transformations as sources of N2O in order to determine how temporal shifts in
these processes affect overall N2O emissions.
One particularly timely topic, as marshes along an estuarine gradient face
rising sea levels, is the potential role of salinity and associated sulfate
concentrations in what have historically been freshwater marshes. Strong
Reconsidering Climatic Roles of Marshes
27
potential exists for salt water intrusion to fundamentally alter the
biogeochemistry of fresh marshes by increasing rates at which organic matter
is mineralized by microbes (Weston et al. 2011). Contrary to the dogma that
methane fluxes are low in saline marshes, an experimental test of salt water
intrusion on tidal freshwater marsh soils resulted in a significant increase in
CH4 and CO2 flux rates for periods of 5-6 months, respectively (Weston et al.
2011). By the end of that one year experiment, the total inorganic C flux (as
CH4 and CO2) out of salt-water amended cores was about 37% greater than
from freshwater cores. This increase in total inorganic C flux (as CO2 and
CH4) out of the salt-water amended cores, representing salinity intrusion, than
their freshwater counterparts (Weston et al. 2011). Although this is contrary to
current understanding of the competitive interactions between methanogens
and sulfate-reducing bacteria, the observed increase in CH4 fluxes could
potentially be explained by the presence of substrates, such as methanol and
methylamines, that sulfate-reducing bacteria do not use, the abundance of
organic substrates in general, or heterogeneity in distributions of various
electron acceptors and donors in the sediments (Weston et al. 2011).
Theoretically, declines in methane oxidation could have contributed to the
enhanced CH4 fluxes, but this process was not measured. Increases in sulfate
(with salinity) might be expected to support anaerobic oxidation of methane
(Conrad et al. 1996), although the significance of this process relative to
aerobic oxidation pathways is not known. Notably, sediment cores were
collected prior to plant emergence in the marsh (Weston et al. 2011), in order
to focus on understanding microbial mediation of soil C mineralization, but the
effects of salt water intrusion on marsh ecosystems and the net greenhouse gas
emissions released from them will likely be significantly mediated by plantmicrobe interactions (discussed further below). Another significant
consequence of the increase in sulfide availability in freshwater marshes that
accompanies salt water intrusion, is that sulfide is known to block complete
denitrification (Seitzinger et al. 1983, Sorensen et al. 1980), and may thus
result in increases in N2O fluxes. A major potential mediator of such effects of
sulfide on denitrifying organisms will be the availability of oxidized iron,
which can ameliorate levels of sulfide that accumulate in marsh sediments
(Kristensen and Kostka 2005).
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Serena Moseman-Valtierra
Summary
N2O production via aerobic processes shows negative relationships to
salinity, as high N2O concentrations are frequently observed in fresh portions
of estuaries (with anthropogenic N inputs). However, in estuarine sediments,
increases in salinity can increase NH4+ fluxes from sediments, which may
indirectly promote nitrification, while denitrification rates were found to
decline (Giblin et al. 2010). Work is needed to characterize the impacts of
such salinity changes on N2O fluxes, but hypothesized results are summarized
in Table 4. Also, sulfide (which accompanies increases in salinity) is known to
block complete denitrification, yielding higher N2O fluxes (Table 4). For
methane, increased salinity has conventionally been thought to inhibit
methanogens, although recent work suggests that methane fluxes from the salt
marshes can be substantial (Moseman-Valtierra et al. 2011, Table 2) and a
laboratory study has found significant, prolonged increases in methane
following increases in salinity (Weston et al. 2011). Methane consumption, on
the other hand, is known to be linked in some cases to sulfate reduction in
microbial consortia (Conrad 1996), although direct links to salinity are not
well characterized and have not been isolated from impacts on
methanogenesis.
TEMPERATURE
Because microbial respiration rates increase with higher temperatures
(Kirwan and Blum 2011), greenhouse gas emissions that result from
respiration would be reasonably expected to increase in response to warming
of marshes. Several studies have documented seasonal patterns of respiration,
methane (Sha et al. 2011, Hirota et al. 2007, Gross et al. 1993, Bartlett et al.
1987), and nitrous oxide fluxes in marshes (Moseman-Valtierra et al. 2011,
Ferron et al. 2007) that are consistent with higher gas emissions in fall and
summer months when temperatures are warmest. For instance, in riverine
wetlands, methane emissions in fall and summer were significantly higher than
winter or spring but did not significantly differ from each other (Sha et al.
2011). A significant positive relationship was observed overall between soil
temperate and methane emissions in 3 of 4 wetlands studied (Sha et al. 2011)
while it was not observed in a created oxbow wetland with low methane
fluxes. The positive relationship between methane and temperature has been
described repeatedly in prior studies (Kim et al. 1999, Chen et al. 2008, Nahlik
Reconsidering Climatic Roles of Marshes
29
and Mitsch 2010). Positive relationships have also been found between N2O
fluxes and either air or soil temperatures at 5 cm depths (Yu et al. 2007) in
freshwater marshes. Soil temperatures in that marsh ranged from close to 0 oC
to nearly 20 oC over the course of the year (Yu et al. 2007).
Preliminary studies have also shown that organic matter decomposition
rates increase by about 20% per each degree of warming, which is about 6
times faster than observed stimulation of marsh productivity (Kirwan and
Blum 2011), although no measurements were made of the greenhouse gases
produced by that respiration. Surprisingly, an experimental warming of a
freshwater Phragmites australis marsh found no effect of a 2.8-2.9 oC increase
in water temperature. This temperature increase, though significant, is just a
fraction of the range experienced over seasonal cycles in temperate marshes
(which can range from 0 to 25 oC, as in Sha et al. 2011), which may explain
the lack of relationship between temperature and methane, and the warming
seemed to be maintained for just a few weeks at a time. However, other factors
besides temperature (such as labile C availability) were suggested to have
limited methanogenesis (Flury et al. 2010).
The effects of temperatures on greenhouse gas emissions may also
manifest via freeze-thaw processes. In sediments of a freshwater marsh, a peak
in N2O emission was observed under low redox conditions (0 to -150 mV),
and were attributed to freezing-thawing effects in the soil. Specifically, the ice
layer above the marsh surface was thought to limit oxygen transport from the
atmosphere to the soil, sealing an organic rich, anoxic layer beneath the
surface, where denitrification could occur (Yu et al. 2007). N2O is known to be
able to be produced at temperatures around 0 oC (Sommerfeld et al. 1993), and
some studies have found that N2O at -4 oC is not different than that at 10-15 oC
(Oquist et al. 2004). Thawing of soils then releases N2O that has been stored
beneath ice in unfrozen sub-surface soils (Bremner et al. 1980). Any impacts
of freeze-thaw cycles on dissolved inorganic nitrogen or labile C availability
would also affect nitrous oxide and possibly methane release from marsh soils.
Summary
Positive relationships have typically been found between temperature and
net greenhouse gas fluxes in the field (Table 4), suggesting that over the time
and space scales of those studies, that increases in temperature may stimulate
microbial production more than microbial consumption of N2O and CH4. In
part, some stimulation of gas fluxes may occur during thawing of ice, which
30
Serena Moseman-Valtierra
physically releases gases from marsh soils. Experimental manipulations of
temperature by just a few degrees Celsius have not significantly influenced
methane emissions although few studies overall have been conducted.
PLANT INFLUENCES
Microbial communities that produce greenhouse gas emissions interact
intimately with vascular plants. Plants release between 20-90% of methane
emissions from wetlands (King et al. 1998). The interactions of macrophytes
and soil microbial processes in methane emission from wetlands have been
reviewed in detail elsewhere (Laanbroek 2010) and will be only briefly
addressed here. The adaptations that have enabled plants to thrive in water
saturated soils of wetlands, aerenchyma and internal gas lacunas, by
transporting oxygen from the atmosphere to soils also play key roles in their
abilities to facilitate transport of gases in the opposite direction (from soils to
the atmosphere). In the wetland reed, Phragmites australis, advective methane
transport was coarsely estimated to be comparable to ebullition rates (Flury et
al. 2010). By oxygenating the soils, plants may also inhibit methanogenesis
because the methane may be oxidized before it reaches the atmosphere
(Laanbroek 2010). Oxygenation also replenishes alternative electron acceptors
which fuels more energetically efficient (and more competitive) respiratory
pathways in the marsh microbial communities (Laanbroek 2010). Specifically,
iron cycling can be notably enhanced in plant rhizospheres and where this is
the case, methane production is likely to be repressed. Potential iron reduction
rates are higher in washed excised roots of freshwater plants (P. cordata, S.
eurycarpum, and T. latifolia) than in salt marsh plants (S. alterniflora) and
seagrasses (Zostera marina) (Laanroek 2010, King and Garey 1999). Ironreducing bacteria are thought to outcompete methanogens and other
heterotrophic bacteria (sulfate reducers) for the organic carbon in rhizospheres
(Laanbroek 2010), although studies in wetlands suggest that recent
photosynthetic products are less significant sources of C fueling methane
production than those derived from plant litter (Megonigal et al. 1996,
Juutinen et al. 2003, Laanbroek 2010). In Patuxuent River (Maryland) iron
reduction rates were higher in tidal freshwater marshes dominated by
Peltandra virginica, Pontederia cordata, and Nuphar lutuem than in brackish
marshes with S. alterniflora, S. patens, and Distichlis spicata (Neubauer
2005). Active iron reduction, influenced by plant rhizosphere effects,
Reconsidering Climatic Roles of Marshes
31
translated into limited rates of methanogenesis within the freshwater marsh
(Neubauer 2005).
Several studies have addressed the influence of plants by examining
relationships between the presence or absence of vegetation and greenhouse
gas emissions. When emergent vegetation was removed from one zone of an
experimental freshwater marsh and compared to a zone with intact plants, no
impact on methane emissions was observed (Altor and Mitsch 2008), however
methane fluxes were positively related to net primary productivity in a
naturally colonizing marsh (Sha et al. 2011). In mesocosm studies of a
brackish marsh in China, S. alterniflora (an invasive) and native P. australis
plants were both found to contribute significantly to methane emissions from
soils (Cheng et al. 2007). Plant biomass and density was significantly
correlated with CH4 emissions, although methane fluxes did not differ between
the species (Cheng et al. 2007). However, when plants of both species were
clipped, N2O emissions increased (Cheng et al. 2007). This suggests that
plants can influence N2O emissions via competition with microbes for nitrogen
in marsh soils.
In general, plant species are known to vary in the magnitude of their
rhizosphere effects, and therefore changes in plant community composition
can influence the greenhouse gas emissions that they facilitate (Laanbroek
2010, Ding et al. 2005, Van der Nat and Middleburg 2000). For example, in
comparisons of the effects of three freshwater marsh plants on methane
emissions, cyperaceous plants (Carex lasiocarpa and Carex meyeriana) were
found to have higher gas transport capacity than a gramineous plant (Deyeuxia
angustifola) (Ding et al. 2005). Native plants differ in their effects on
greenhouse gas emissions from invasive plants also. In mesocosm studies, the
native plant of a coastal salt marsh in China, Suaeda salsa, was found to
support much lower rates of methane emissions than Spartina alterniflora,
which is invasive in that region (Zhang et al. 2010). Similar results were found
for both CH4 and N2O emissions, which were higher in mesocosms of a
brackish marsh with invasive Spartina alterniflora than a native, Phragmites
australis. The main reason for these differences, in both studies, was higher
plant biomass of S. alterniflora (Zhang et al. 2010). The plant biomass was
thought to be related to more organic C for methanogens in the invaded marsh
soil than in that with the native plant (Zhang et al. 2010). Enhancement of the
biomass and stem density of S. alterniflora, via N addition, resulted in
stimulation of CH4 emissions by 71.7% (Zhang et al. 2010).
Although vascular plants stimulate greenhouse gas emissions through
exudation of labile carbon, they might-alternatively- limit them via
32
Serena Moseman-Valtierra
oxygenation of rhizospheres in cases where anaerobic processes dominate
production of N2O and CH4. Research is needed to clarify which factors
control the relative balance of these seemingly opposing processes.. In some
cases, oxygenation can actually promote N2O emissions, as in a wetland
constructed for wastewater removal in which plant species stimulated
nitrification to in their rhizospheres, with Zizania latifolia promoting more
nitrification and N2O emissions than Phragmites australis and Typha latifolia
(Wang et al. 2008). Overall, the direction of plant impacts on GHG fluxes
could be determined not only by plant species composition, but also by the
physiological states of the plants, which can alter relative levels of
oxygenation or C exudation (Lovell 2005). The net influence of plants on
greenhouse gas emissions likely also depends upon the composition of
microbial communities that reside in marsh sediments (including the
prevalence of autotrophs versus heterotrophs) at a given time. Further studies
are needed to describe the distribution and controls on microbial populations
involved in production or consumption of methane and nitrous oxide. What
seems clear is that, on successional time scales, marshes with more developed
plant communities (and higher primary production) constitute bigger net
sources of methane than those with less accumulated organic matter (Nahlik
and Mitsch 2010), but it is less well known how N2O emissions vary with
marsh succession. The latter may depend mostly on anthropogenic N loading
(discussed above). Thus the general relationship between plant productivity
and the net global warming potential of marsh ecosystems is not yet clear.
Intriguingly, relationships between plant biomass or productivity metrics
and greenhouse gas emissions may facilitate landscape-scale estimates of these
emissions. For example, positive relationships between Typha biomass in
brackish marshes and dissolved methane porewater concentrations have been
proposed for use in remote sensing estimates of CH4 (Gross et al. 1993).
Successful implementation of such measurement approaches will require
better understanding of the relationships between plant physiology and
greenhouse gas emissions in marshes.
Compared to vascular plants, relatively fewer studies seem to have
addressed the role of algae or epiphytes in mediating greenhouse gas
emissions from marshes. Algae may have interesting indirect effects on
greenhouse gas emissions by influencing oxygen levels of sediments, or
contributing to organic C sources in marsh soils, particularly as algal litter is
less refractory than that of vascular plants. In contrasts of chambers with and
without algal mats, in coastal sediments influenced by anthropogenic nitrogen
inputs, more N2O consumption was found in the presence of algae
Reconsidering Climatic Roles of Marshes
33
(LaMontagne et al. 2003). The hypoxic conditions created by the algal mat
were thought to promote use of N2O as an electron acceptor by microbes
(completing denitrification) (LaMontagne et al. 2003). Epiphytes on
macroalgal fronds have also been found to produce N2O when exposed to high
nitrate concentrations of 550-950 M (Law et al. 1993). Microniches may
exist in which nitrate concentrations occasionally reach those levels, perhaps if
nutrient inputs from groundwater are sealed beneath algal mats, limiting
dilution with overlying water. Also, epiphytes on dominant macrophytes were
found to have comparable denitrification potentials to those measured in
sediments (Bourgues and Hart 2007), which suggests that N2O production
might be notable by these organisms. In contrast, no known studies have
documented strong links between algae and methane emissions in marshes.
FAUNAL INFLUENCES
Animals in marshes may directly constitute sources of greenhouse gases,
although their largest effects may be via indirect influences associated with
feeding activities that change the structure, texture, and chemical composition
of marsh soils and sediments. In coastal sediments, burrowing macrofauna can
reach sufficient densities to significantly contribute to N2O emissions from
sediments (Stief et al. 2009). Microbes in the guts of these animals were found
to be major sources of N2O emissions, and although similar studies are not
known to have examined this for methane in marshes specifically, certainly
methanogens thrive among gut microflora. In environments with high densities
of macrofauna, gut microbes may rival or exceed their sedimentary
counterparts as sources of greenhouse gases, but their overall contribution to
fluxes in marshes and other wetlands remain to be quantified. In coastal
sediments, bioirrigation activities of animals introduce oxygen into otherwise
anoxic sediments, increasing the area and depth of oxic-anoxic boundaries
across which nitrification and denitrification can be coupled (reviewed in
Kristensen and Kostka 2005, Figure 1). Macrofauna also excrete ammonium,
urea, and organic-rich deposits (of feces and pseudofeces) that fuel microbial
populations in sediments, or tubes or burrows (Barnes and Owens 1998,
Mermillod-Bloadin et al. 2008). High denitrification rates have repeatedly
been found in sites with high densities of macrofauna (i.e. Barnes and Owens
1998), and these may be sources of N2O.
For methane, oxic-anoxic boundaries may promote methane oxidation,
thereby decreasing net CH4 emissions relative to coastal sediments or marsh
34
Serena Moseman-Valtierra
soils that are relatively depauperate of macrofauna. Swan foraging, for
example, was found via field enclosures, to decrease methane production in
freshwater temperate wetlands because the bioturbation increased methane
oxidation rates while decreasing methanogenesis (Bodelier et al. 2006). The
grazing activities may have a role in stimulating release of methane from
sediments, however, which may partially compensate for the reduction in
methane emissions due to those effects (Bodelier et al. 2006, Dingemans et al.
2011). The swans also indirectly diminished methane emissions by reducing
the density of a fennel pondweed, Potamogeton pectinatus, which would have
stimulated methane production via exudation of labile C (Bodelier et al. 2006).
Although the swans had no effect on ammonium oxidation, activities of
muskrats (grazing, burrowing, lodging construction), were found to stimulate
potential net nitrogen mineralization and nitrification in a freshwater tidal
marsh (Connors et al. 2000). The latter indicates that N2O fluxes can
potentially be affected by large grazers. In contrast to the effects of swans,
methane and CO2 emissions were found to be higher at low tides from tropical
coastal sediments with fiddler crab burrows and mangrove pneumatophores
(aerial roots) than they were in bare sediments (Kristensen et al. 2008), likely
because these structures act as conduits through which the gases are released.
Indirect trophic effects of animals on plants that mediate greenhouse gas
emissions are also possible, although current work is needed to first better
understand the mechanisms and magnitudes of direct effects of both plants and
animals on these biogeochemical processes.
PREDICTIONS FOR THE FUTURE
Mechanistic understanding of greenhouse gas emissions from ecosystems
is vital for predicting ways that management practices may help to ameliorate
anthropogenic climate change and sustain marshes against multiple aspects of
global change. As marshes continue to be considered for emerging carbon
markets, incentives to maximize biological carbon sequestration will increase,
along with the need to predict, monitor, and minimize losses of CO2, N2O, and
CH4 from marsh soils and waters to the atmosphere. Meanwhile, the microbial,
plant, and animal communities in marshes may be shifting in response to
biological invasions, warming climates, rising sea levels, salt water intrusion,
and anthropogenic nitrogen inputs. Current research needs to address how
these factors independently and interactively affect wetland communities and
biogeochemical functions of marshes.
Reconsidering Climatic Roles of Marshes
35
Anthropogenic perturbations to the global nitrogen cycle are likely to
enhance greenhouse gas emissions from marshes, particularly CO2 and N2O,
by stimulating respiration (Wigand et al. 2009) and denitrification rates in
marsh soils (Moseman-Valtierra et al. 2011), as they have in numerous other
ecosystems (Liu and Greaver 2009). In marsh soils that are highly ammonium
enriched, methane emissions may also increase, if methane oxidation is
inhibited, although the response may be constrained by pH (given that
methane emissions are highest near neutral pH). Over the long periods in
which most coastal ecosystems are experiencing eutrophication from
anthropogenic N inputs, both plant and microbial communities can shift,
which may change the magnitude of greenhouse gas emissions from particular
marshes or zones, as well as they way that those gas fluxes vary with changing
environmental conditions. One remaining challenge is predicting how much
greenhouse gases will change in marshes in response to N loading is to
specifically identify the microbial communities and particular pathways that
are responsible for the emissions. Doing so may help to explain some of the
remarkable heterogeneity observed in N2O and CH4 fluxes, for instance,
particularly in chronically fertilized marshes (Moseman-Valtierra et al. in
prep).
Although marsh community composition may be varying in response to
anthropogenic N loading, the “face” of marshes is also rapidly changing as
invasive species spread. Particularly in coastal marshes, biological invasions
may dramatically alter the structure and function of the ecosystem, including
greenhouse gas emissions. Studies reviewed above indicate that the massive,
dominant invasive plants that are spreading in marshes tend to facilitate
greater greenhouse gas emissions than the native species that they outcompete.
Nutrient loading is known to facilitate several biological invasions (Bennett et
al. 2011, Marton and Wasson 2008, Rickey and Anderson 2004) and thus as N
loading is enhancing greenhouse gas production in soils, invasive plants may
further promote transmission of those gases from anoxic muds to the
atmosphere. Invasive animals, particularly those which generate biogenic
structures, such as crabs or burrowing isopods, are also very likely to be
changing greenhouse gas emissions, although more studies are needed to be
able to quantify the extent and direction of those alterations. Hypoxic
conditions in coastal sediments reduce the numbers and size of burrowing
infauna (Diaz and Rosenberg 1999), which would minimize the oxygenated
surface areas and lead to increases in sulfide, and possibly decreased in pH, in
coastal marshes. This may increase N2O emissions, due to incomplete
denitrification, and favor methanogenesis via the loss of oxic microniches.
36
Serena Moseman-Valtierra
Further, as rising sea levels increase the extent and duration of marsh
inundation they may reduce oxygen levels in marsh soils along lower elevation
zones and increase the spatial extent of sulfate (and sulfide) along estuarine
gradients, further stimulating greenhouse gas emissions (Larsen et al. 2011).
Although more studies are needed to predict how sea level rise will affect
marshes, in terms of shifting plant and animal communities, data thus far have
surprisingly shown that increases in salinity can increase methane emissions
from marsh soils and accelerate organic matter remineralization rates (Weston
et al. 2011). Thus the carbon that is intended to be stored in wetlands may not
be neatly sealed beneath the rising sea, but rather it may be emitted back to the
atmosphere in the form of greenhouse gases, potentially exacerbating
anthropogenic climate change.
To test hypotheses such as these, regarding the biogeochemical responses
of marshes to complex environmental changes, interdisciplinary approaches
and innovative technology are needed which can not only detect dynamic
changes in greenhouse gas emissions but also quantify, manipulate, and model
those gas fluxes. Automated sampling platforms that can simultaneously detect
changes in CO2, CH4, and N2O at high spatial and temporal resolutions will be
required to constrain the heterogeneity of these greenhouse gas emissions from
dynamic marsh ecosystems. Such systems need to be precise but also
economical, so that resource managers can accurately assess impacts of
restoration projects and other watershed management practices on greenhouse
gas emissions. Although relatively few studies thus far have simultaneously
quantified all 3 greenhouse gases in marshes, they do need to be measured
together in order to ascertain the net global warming potential (GWP) of these
ecosystems. Ideally these measurements would be coordinated, in tandem with
climatic measurements and studies of C sequestration rates, across a range of
marsh types through coordinated research networks that span latitudinal and
climatic gradients. While challenging, this area of research offers a promising
opportunity for scientists to think and work across spatial and temporal scales,
explicitly considering the interactions of microbial cells with plant and animal
assemblages in marshes that may ultimately exert influences on global climate.
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